Lipopolysaccharide Transport System Links Physiological Roles of σE and ArcA in the Cell Envelope Biogenesis in Shewanella oneidensis
ABSTRACT The bacterial cell envelope is not only a protective structure that surrounds the cytoplasm but also the place where a myriad of biological processes take place. This multilayered complex is particularly important for electroactive bacteria such as Shewanella oneidensis, as it generally hos...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2021-09-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/Spectrum.00690-21 |
| _version_ | 1798035779213066240 |
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| author | Peilu Xie Huihui Liang Jiahao Wang Yujia Huang Haichun Gao |
| author_facet | Peilu Xie Huihui Liang Jiahao Wang Yujia Huang Haichun Gao |
| author_sort | Peilu Xie |
| collection | DOAJ |
| description | ABSTRACT The bacterial cell envelope is not only a protective structure that surrounds the cytoplasm but also the place where a myriad of biological processes take place. This multilayered complex is particularly important for electroactive bacteria such as Shewanella oneidensis, as it generally hosts branched electron transport chains and numerous reductases for extracellular respiration. However, little is known about how the integrity of the cell envelope is established and maintained in these bacteria. By tracing the synthetic lethal effect of Arc two-component system and σE in S. oneidensis, in this study, we identified the lipopolysaccharide transport (Lpt) system as the determining factor. Both Arc and σE, by regulating transcription of lptFG and lptD, respectively, are required for the Lpt system to function properly. The ArcA loss results in an LptFG shortage that triggers activation of σE and leads to LptD overproduction. LptFG and LptD at abnormal levels cause a defect in the lipopolysaccharide (LPS) transport, leading to cell death unless σE-dependent envelope stress response is in place. Overall, our report reveals for the first time that Arc works together with σE to maintain the integrity of the S. oneidensis cell envelope by participating in the regulation of the LPS transport system. IMPORTANCE Arc is a well-characterized global regulatory system that modulates cellular respiration by responding to changes in the redox status in bacterial cells. In addition to regulating expression of respiratory enzymes, Shewanella oneidensis Arc also plays a critical role in cell envelope integrity. The absence of Arc and master envelope stress response (ESR) regulator σE causes a synthetic lethal phenotype. Our research shows that the Arc loss downregulates lptFG expression, leading to cell envelope defects that require σE-mediated ESR for viability. The complex mechanisms revealed here underscore the importance of the interplay between global regulators in bacterial adaption to their natural inhabits. |
| first_indexed | 2024-04-11T21:01:52Z |
| format | Article |
| id | doaj.art-64b0397c94c24837a859d5e868c74a07 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-11T21:01:52Z |
| publishDate | 2021-09-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-64b0397c94c24837a859d5e868c74a072022-12-22T04:03:27ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972021-09-019110.1128/Spectrum.00690-21Lipopolysaccharide Transport System Links Physiological Roles of σE and ArcA in the Cell Envelope Biogenesis in Shewanella oneidensisPeilu Xie0Huihui Liang1Jiahao Wang2Yujia Huang3Haichun Gao4Institute of Microbiology and College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, ChinaInstitute of Microbiology and College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, ChinaInstitute of Microbiology and College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, ChinaInstitute of Microbiology and College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, ChinaInstitute of Microbiology and College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, ChinaABSTRACT The bacterial cell envelope is not only a protective structure that surrounds the cytoplasm but also the place where a myriad of biological processes take place. This multilayered complex is particularly important for electroactive bacteria such as Shewanella oneidensis, as it generally hosts branched electron transport chains and numerous reductases for extracellular respiration. However, little is known about how the integrity of the cell envelope is established and maintained in these bacteria. By tracing the synthetic lethal effect of Arc two-component system and σE in S. oneidensis, in this study, we identified the lipopolysaccharide transport (Lpt) system as the determining factor. Both Arc and σE, by regulating transcription of lptFG and lptD, respectively, are required for the Lpt system to function properly. The ArcA loss results in an LptFG shortage that triggers activation of σE and leads to LptD overproduction. LptFG and LptD at abnormal levels cause a defect in the lipopolysaccharide (LPS) transport, leading to cell death unless σE-dependent envelope stress response is in place. Overall, our report reveals for the first time that Arc works together with σE to maintain the integrity of the S. oneidensis cell envelope by participating in the regulation of the LPS transport system. IMPORTANCE Arc is a well-characterized global regulatory system that modulates cellular respiration by responding to changes in the redox status in bacterial cells. In addition to regulating expression of respiratory enzymes, Shewanella oneidensis Arc also plays a critical role in cell envelope integrity. The absence of Arc and master envelope stress response (ESR) regulator σE causes a synthetic lethal phenotype. Our research shows that the Arc loss downregulates lptFG expression, leading to cell envelope defects that require σE-mediated ESR for viability. The complex mechanisms revealed here underscore the importance of the interplay between global regulators in bacterial adaption to their natural inhabits.https://journals.asm.org/doi/10.1128/Spectrum.00690-21lipopolysaccharide transport systemArc regulatory systemσEcell envelopeenvelope stress responseregulation |
| spellingShingle | Peilu Xie Huihui Liang Jiahao Wang Yujia Huang Haichun Gao Lipopolysaccharide Transport System Links Physiological Roles of σE and ArcA in the Cell Envelope Biogenesis in Shewanella oneidensis Microbiology Spectrum lipopolysaccharide transport system Arc regulatory system σE cell envelope envelope stress response regulation |
| title | Lipopolysaccharide Transport System Links Physiological Roles of σE and ArcA in the Cell Envelope Biogenesis in Shewanella oneidensis |
| title_full | Lipopolysaccharide Transport System Links Physiological Roles of σE and ArcA in the Cell Envelope Biogenesis in Shewanella oneidensis |
| title_fullStr | Lipopolysaccharide Transport System Links Physiological Roles of σE and ArcA in the Cell Envelope Biogenesis in Shewanella oneidensis |
| title_full_unstemmed | Lipopolysaccharide Transport System Links Physiological Roles of σE and ArcA in the Cell Envelope Biogenesis in Shewanella oneidensis |
| title_short | Lipopolysaccharide Transport System Links Physiological Roles of σE and ArcA in the Cell Envelope Biogenesis in Shewanella oneidensis |
| title_sort | lipopolysaccharide transport system links physiological roles of σe and arca in the cell envelope biogenesis in shewanella oneidensis |
| topic | lipopolysaccharide transport system Arc regulatory system σE cell envelope envelope stress response regulation |
| url | https://journals.asm.org/doi/10.1128/Spectrum.00690-21 |
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